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Home , Bathymodiolus, Protolira, Rainbow Vent Field

evidence for serpentinization fluids fueling chemosynthetic assemblages

Franck Lartauda,b,1, Crispin T. S. Littlec, Marc de Rafelisb, Germain Bayond, Jerome Dymente, Benoit Ildefonsef, Vincent Gressierb, Yves Fouquetd, Françoise Gaillg, and Nadine Le Brisa,h

aUniversité Pierre et Marie Curie–Paris 6, Laboratoire d’Ecogéochimie des Environnements Benthiques, Centre National de la Recherche Scientifique, Laboratoire Arago, 66650 Banyuls-sur-Mer, France; bUniversité Pierre et Marie Curie–Paris 6, Institut des Sciences de la Terre de Paris, Laboratoire Biominéralisations et Environnements Sédimentaires, Centre National de la Recherche Scientifique 75252 Paris Cedex 05, France; cSchool of Earth and Environment, University of Leeds, Leeds LS2 9JT, United Kingdom; dDépartement Géosciences Marines, Institut Français de Recherche pour l’Exploitation de la Mer, Centre de Brest, 29280 Plouzané, France; eInstitut de Physique du Globe de Paris, Centre National de la Recherche Scientifique, Equipe Géosciences Marines, 75252 Paris Cedex 05, France; fGéosciences Montpellier, Centre National de la Recherche Scientifique, Université Montpellier 2, 34095 Montpellier Cedex 05, France; gCentre National de la Recherche Scientifique, Institut Écologie et Environnement, Université Pierre et Marie Curie, Institut de Recherche pour le Développement, Muséum National d’Histoire Naturelle, 75252 Paris Cedex 05, France; and hLaboratoire Environnements Profonds, Institut Français de Recherche pour l’Exploitation de la Mer, Centre de Brest, 29280 Plouzané, France

Edited by Norman H. Sleep, Stanford University, Stanford, CA, and approved March 24, 2011 (received for review June 30, 2010)

Among the deep-sea sites discovered in the vent fluids are -poor, low-temperature (40–91 °C), and past 30 years, Lost City on the Mid-Atlantic Ridge (MAR) is have high pH (9–11). Further, the Lost City fluids are also highly remarkable both for its alkaline fluids derived from mantle rock enriched in H2 and CH4 and comparatively lower in H2S (10). serpentinization and the spectacular seafloor carbonate chimneys On contact with ambient seawater these alkaline fluids precipi- precipitated from these fluids. Despite high concentrations of tate chimney structures up to 60 m high composed of carbonates reduced chemicals in the fluids, this unique example of a serpenti- (aragonite and calcite) and brucite (MgðOHÞ2) (11–13). Sulfide nite-hosted hydrothermal system currently lacks chemosynthetic minerals are mostly absent from these chimneys, contrasting assemblages dominated by large typical of high-tempera- strongly with on-axis hydrothermal vent structures (13, 14). The ture vent sites. Here we report abundant specimens of chemosym- Lost City site has generated considerable interest because this biotic , associated with gastropods and chemosymbiotic sort of system was likely to have been common in early Earth his- clams, in approximately 100 kyr old Lost City-like carbonates from tory and represents a plausible geochemical environment for the the MAR close to the Rainbow site (36 °N). Our finding shows that emergence of life on this, and potentially other, planets (15, 16). serpentinization-related fluids, unaffected by high-temperature In the context of the MAR -hosted vent fields hydrothermal circulation, can occur on-axis and are able to sustain another remarkable feature of Lost City is the lack of typical high-biomass communities. The widespread occurrence of seafloor high-biomass assemblages dominated by large chemosyn- ultramafic rocks linked to likely long-range dispersion of vent thetic invertebrates: There are currently no Bathymodiolus mus- species therefore offers considerably more ecospace for chemosyn- sel beds or bresiliid shrimp swarms, although the diversity of thetic fauna in the oceans than previously supposed. other invertebrates (particularly small gastropods and polychaete worms) is described as being equivalent to that of high-tempera- Bathymodiolus ∣ Ghost City ∣ ultramafic-hosted ∣ mid-ocean ridge ∣ ture MAR vent communities (11, 17). Only two living specimens ecogeochemistry of Bathymodiolus aff. azoricus have been found at Lost City (18, 19), whereas hundreds of broken shell fragments downslope igh-temperature hydrothermal vents occur at very geographi- away from the active chimney areas (19, 20) suggest that the Hcally restricted sites in the deep-sea, localized on spreading population size might have been much larger in the past and is ridges and arc-related volcanoes. Typically, such vent fluids are now almost extinct (19). Dead B. azoricus shells have also been metal- and H2S-rich and precipitate metallic sulfide chimneys on recently reported from carbonate chimneys at an inactive site the seafloor (1, 2). These vents usually support high-biomass near Lost City (21). invertebrate communities, dominated by a small number of Supporting these observations, the enrichment of reduced endemic species forming symbioses with diverse chemoauto- compounds in Lost City hydrothermal fluid indicates that these, trophic (e.g., siboglinid tubeworms, bresiliid shrimp, and similar peridotite-hosted vents, hold the energetic potential provaniid gastropods, vesicomyid clams, and bathymodiolin to support large aggregations of Bathymodiolus mussels, a mussels) (1, 3). These symbioses exploit chemical energy from widely distributed along the MAR axis (22). B. aff. azoricus at a variety of fluids enriched in reduced compounds, mostly hydro- Lost City hosts the same symbiont phylotypes as the methano- gen sulfide and , to fix carbon (4). Along slow and trophic and thiotrophic endosymbionts of both B. azoricus and ultraslow spreading ridges, like the Mid-Atlantic Ridge (MAR), B. puteoserpentis from on-axis sites on the MAR (18), where the ultramafic mantle rocks can be exposed on the seafloor by large methanotrophic symbiont fixes carbon from methane and the offset faults (5). Seawater serpentinization of these chemolithoautotroph uses sulfide to fix CO2 (23–25). In addition produces , which subsequently reacts with CO2 to form to methane, DeChaine et al. (18) suggest that B. aff. azoricus at methane (6, 7). Because of this, peridotite-hosted high-tempera- Lost City could also be utilizing hydrogen, although hydrogen-oxi- ture vent sites on the MAR (e.g., Rainbow and Logatchev) exhibit dizing symbionts have yet to be identified. These authors further elevated levels of methane and hydrogen contents in their fluids.

Hydrothermal activity can also occur at off-axis ridge settings. Author contributions: F.L., M.d.R., J.D., B.I., Y.F., F.G., and N.L.B. designed research; F.L., A unique example of this is the Lost City vent field, discovered C.T.L., M.d.R., G.B., and V.G. performed research; F.L., C.T.L., M.d.R., G.B., and N.L.B. in the year 2000 on the Atlantis Massif, 30°07′N MAR, at 750- to analyzed data; and F.L., C.T.L., and N.L.B. wrote the paper. 850-m depth (8). Here, exothermic serpentinization processes The authors declare no conflict of interest. may largely drive the hydrothermal convection, although a This article is a PNAS Direct Submission. contribution of magmatic inputs is not excluded (9). The main 1To whom correspondence should be addressed. E-mail: [email protected]. difference between this off-axis vent field and the other known This article contains supporting information online at www.pnas.org/lookup/suppl/ vent fields on the MAR-axis is that the majority of the Lost City doi:10.1073/pnas.1009383108/-/DCSupplemental.

7698–7703 ∣ PNAS ∣ May 10, 2011 ∣ vol. 108 ∣ no. 19 www.pnas.org/cgi/doi/10.1073/pnas.1009383108 Downloaded by guest on September 29, 2021 suggested that hydrogen sulfide would be poorly available for from the northwestern flank of the Rainbow massif, which is mussels at Lost City (18), based on measured sulfide concentra- situated on a nontransform offset at 36°14.15N, 33°53.50W (Fig. 1 tions from Lost City end-member fluids. However, this hypothesis and Fig. S1). This site, which we name Ghost City, is 1,200 m is not supported by the comparison of the end-member total dis- northeast of the Rainbow vent field at around 2,100 m water solved sulfide versus temperature ratios between Lost City and depth. The dredge from which the carbonates were collected the on-axis vent fields (Table S1). The maximum temperature sampled a transect around 800 m long on the seafloor and recov- of the habitat of Bathymodiolus mussels lies around 15 °C, and it ered, in addition to the carbonates, three shells of thyasirid requires significant dilution of the end-member fluids in cold bivalves, numerous pieces of serpentinized peridodite, and some seawater. In this temperature range, the sulfide concentration troctolites and . The carbonates are white to ivory in resulting from the dilution of Lost City end-member fluids should color, ranging from 750 to 25 cm3 in volume, and most have thin be rather similar to the levels experienced by mussels from on-axis (up to 1 mm) exterior ferric oxyhydroxide (ferrihydrite with Mn vent fields (22, 26). Recent data (27), moreover, suggest that component) black crusts upon which solitary corals have grown fluids issuing from flanges on the flanks of Lost City chimneys (Fig. 2 A and B and Fig. S2). The carbonate textures range from may indeed have a higher H2S∕temperature ratio than the end- “layered” (Fig. 2C and Fig. S3), with significant porosity (close to member fluid. Given the potential availability of these reduced 40%, n ¼ 4), to “massive.” This carbonate matrix, which encloses 3 compounds in the Lost City vent fluids for symbionts and free- shells with a density of up to 4 shells per 10 cm , lacks living chemotrophic microbial populations (28, 29), there is there- metallic oxide or sulfide minerals and consists of varying propor- fore no reason to suppose that Lost City-type fluids should ex- tions of authigenic carbonate cements and infilling pelagic calcitic clude the formation of dense chemosynthetic faunal assemblages. and aragonitic (foraminifera, coccoliths, and a few ptero- The findings contained in this paper support the hypothesis pods; Fig. 2D and Fig. S3). The authigenic carbonate cements that Lost City-type fluids can sustain such communities, while pro- consist of aragonite, commonly occurring as radial aggregates of viding further evidence for the suggestions of Kelley et al. (17, 30) acicular crystals, calcite, and sparser rosettes of glendonite crys- that low-temperature hydrothermal circulation on slow-spreading tals (Fig. 2 E and F and Fig. S4). The infilling pelagic sediments 18 13 ridges has a widespread distribution. We report previously unre- have δ O values of 3.63 0.25‰ and δ C values of 0.93 ported Lost City-like carbonates containing fossil Bathymodiolus 0.17‰ (n ¼ 4). Mixed calcite/aragonite authigenic cements have 18 13 shells of large size at high densities, together with smaller numbers δ O and δ C values of 4.88 0.19‰ and −0.66 1.18‰, of two species of chemosynthetic bivalves and four gastropod respectively (n ¼ 9) (Table 1). The authigenic carbonates and species. This fossil assemblage is 110,000 years old (based on the infilling pelagic sediment show good separation between 13 18 radiogenic isotopes) and contains similar species to the Bathymo- δ C and δ O on a canonical discriminant analysis (CDA) scat- diolus mussel beds from high-temperature vents elsewhere on the terplot, supporting distinct mineralization process (Fig. 3 and MAR. Although geographically close to the Rainbow hydrother- Table S2). Isotopic measurements of a series of subsamples from mal vent field, the Ghost City carbonates and fossils were clearly one authigenic carbonate crust gave U∕Th ages ranging from 46 0.3 kyr to 193 11 kyr (n ¼ 4) (Table 2). These samples, associated with a distinct type of environment associated with 234 metal-poor fluid venting, contrasting with all known MAR-axis however, display a wide range of initial δ U values (from high-temperature vent fluids. This finding not only reveals the ex- approximately 129 to 183‰), suggesting that their U∕Th ages istence of low-temperature hydrothermal circulation in serpenti- may be possibly biased due to postformation interaction with nized systems driving substantial fluxes of reduced chemicals close seawater or diagenesis (31). One of these subsamples is charac- δ234 150 1‰ to the ridge axis, but it also expands the range of marine environ- terized by a Uinitial value ( ; Table 2) close to the 146 6 2 6‰ ments that can support chemosynthetic animal communities. modern seawater signature ( . . ) (31), which suggests that its U∕Th ratio may be considered as the most representative Ghost City Carbonates of the formation age of Ghost City carbonates. The correspond- Eight carbonate blocks were dredged during the MoMAR- ing U∕Th age (110 0.9 kyr) lies in the same range as the older DREAM cruise (MoMAR 08 Leg 2, August–September 2008) chimneys from Lost City (122 12 kyr) (32) and suggests that GEOLOGY

Fig. 1. Location of the Ghost City fossil hydrother- mal field at different scales. (A) Large scale map showing hydrothermal vents hosted by volcanic rocks (red dots) and gabbros and peridotites (green dots); Ghost City is in the vicinity of the Rainbow hydrother- mal field. (B) Standard multibeam bathymetrical map of three MAR segments between 36°00 and 36°20N. These segments show a typical slow-spreading axial valley offset by two nontransform discontinuities. Both Rainbow and Ghost City are located at the northern end of the segment centered on 36°10N. (C) High resolution multibeam bathymetric map ac- quired at low ship speed during the Flores cruise of the R/V L’Atalante showing the Rainbow vent field on the western flank of the Rainbow massif; the Ghost City fossil site is located on the northwestern flank of this gabbroic and peridotitic structure approximately 1,200 m northeast of the Rainbow vent field, at a depth of 2,100 m.

Lartaud et al. PNAS ∣ May 10, 2011 ∣ vol. 108 ∣ no. 19 ∣ 7699 Downloaded by guest on September 29, 2021 Fig. 3. Oxygen and carbon isotopic composition of Ghost City carbonates and Bathymodiolus shells and living Bathymodiolus shells from the Rainbow hydrothermal vent field. Domains limited by lines represent the scatterplot of canonical scores obtained by applying discriminant functions to the data.

precipitation associated with aging and are colonized by serpulid worms and corals (13). In older inactive chimneys the internal microchannels are progressively in-filled with micritic calcite; brucite, which is undersaturated in seawater, tends to Fig. 2. Carbonate samples from Ghost City. (A) Sectioned block formed of disappear in these chimneys (12). Another feature indicative of authigenic carbonate cements covered by ferric oxyhydroxide dark crust prolonged postformation interaction with seawater is near sea- upon which (B) solitary corals have grown. (Scale bars, 1 cm.) (C) Photomicro- water Sr isotope values in carbonate minerals, as seen in both the graph showing anastomosing aragonite laminae defining fluid flow channels Lost City inactive chimneys (13) and Ghost City samples. One (center and right) and a piece of mussel shell (bottom left). The channels have thin aragonite walls, some with thin collomorphic coatings; others are mineralogical distinction of Ghost City carbonates is the presence in-filled with micritic carbonate. A thin rim of aragonite acicular crystals of glendonite. Glendonite in Ghost City carbonate crust exhibits seems to be the latest cement phase, covering mussel shells, channel walls a characteristic star shape and is associated with acicular arago- (top left), and micritic infill (center right). (Scale bars, 1 mm.) (D) Photomicro- nite crystals surrounding the benthic fossils. Glendonite is a pseu- graph showing articulated mussel specimens and gastropods enclosed domorph after ikaite, a very unstable hydrous calcium carbonate within authigenic carbonate. (Scale bars, 1 mm.) (E and F) SEM photomicro- associated with cold water (<6 °C) depositional systems, includ- graphs of carbonates showing aragonite acicular crystals (E) and rosette of ing glaciomarine and deep water settings (36, 37). Original ikaite glendonite crystals (F). (Scale bars, 20 μm.) precipitation is favored by elevated alkalinity, high pH (>10) and Ghost City carbonate formation is significantly older than the dissolved phosphate enrichments. Glendonite was not reported first evidence of Rainbow vent activity (23 1.5 kyr) (33). Addi- in Lost City carbonates, but the presence of ikaite in the walls tionally, the same carbonate sample exhibits a radiogenic stron- of active chimneys was suspected from the observation of rapid tium isotopic ratio (87Sr∕86Sr) of 0.70916 0.00006, close to dissolution of elongated carbonate crystals during sampling (13). seawater ratios. The oxygen and carbon isotope values of the Ghost City Among known authigenic carbonates from oceanic environ- authigenic carbonates are consistent with those observed in 18 ments where ultramafic rocks are exposed, such as -filling serpentinization contexts. The O enrichment during fluid/rock 18 aragonites in (34, 35), samples from Ghost City interaction results in carbonates with high δ O values (>2‰) 13 are texturally and mineralogically most similar to those from Lost (11, 38). The Ghost City carbon isotope signatures (δ C ¼ −2.6 City, particularly the carbonates of old (up to 25 kyr) inactive to 0.7‰) are comparable to those measured in carbonates chimneys (12). According to these authors, the Lost City inactive from -hosted systems, like the South Chamorro Sea- structures display well-defined fluid flow paths, retaining signifi- mount (δ13C ¼ −2.1 to −1.3‰) and the Conical Seamount cant porosity (up to approximately 35%) and are characterized (δ13C ¼ −2.9 to −0.1‰) in the Mariana forearc (39–41), and lie by dark or black exteriors that contrast to white, ivory, or gray within the wide range of carbonate isotopic signatures reported interiors. The outer walls of these structures become dark due to for Lost City (−7 to þ13‰) (11). Carbonates with the lower

Table 1. Mean, standard deviation, and range of oxygen and carbon isotopic compositions of carbonates and mussel shells (n) δ18O SD (‰ VPDB) Min∕Max δ13C SD (‰ VPDB) Min∕Max GHOST CITY In-filled pelagic sediments 4 3.63 ± 0.25 3.27∕3.85 0.93 ± 0.17 0.72∕1.09 Authigenic carbonates 9 4.88 ± 0.19 4.48∕5.09 −0.66 ± 1.18 −2.56∕0.67 Bathymodiolus shells 3 4.93 ± 0.40 4.52∕5.31 −0.30 ± 1.99 −2.59∕1.08 LOST CITY Vent carbonates (11) 50 −6∕5 −7∕13 Methane (11, 44, 45) −11.9 −13.6∕−8.8 RAINBOW Living Bathymodiolus shells 5 2.32 ± 0.59 1.67∕2.99 2.78 ± 0.41 2.35∕3.25 Methane (44) −17.7∕−15.8 Comparison of carbonates and mussel shells from Ghost City, Lost City, and Rainbow high-temperature hydrothermal vent site.

7700 ∣ www.pnas.org/cgi/doi/10.1073/pnas.1009383108 Lartaud et al. Downloaded by guest on September 29, 2021 18 13 Table 2. U-Th ages for Ghost City carbonate samples azoricus shells (δ O ¼ 4.93 0.40‰, δ C ¼ −0.30 1.99‰, 234 n ¼ 3; Table 1), values that are more similar to the Ghost City Corrected U-Th age (kyr) Initial δ U(‰) authigenic carbonates than living Bathymodiolus shells from Sample ± 2σ ±2σ the Rainbow high-temperature hydrothermal vent site (CDA S1 195 ± 11 183 ± 10 analysis; Fig. 3 and Table S2). The other benthic fossils enclosed S2 110 ± 0.9 150 ± 1 within the Ghost City carbonate samples (Fig. 4) comprise serpu- S3 65 ± 11 170 ± 1 lid tubes (>30); the vesicomyid clam Phreagena sp. (n ¼ 2); the S4 46 ± 0.3 129 ± 1 thyasirid clam Thyasira sp. (n ¼ 1); the limpet Paralepetopsis aff. ferrugivora (n ¼ 15); and the snails Protolira aff. thorvaldssoni isotopic signature reflect a mixed inorganic carbon source with (n ¼ 32), Phymorhynchus sp. (n ¼ 1), Anatoma sp. (n ¼ 2), and δ13 ∼ 0‰ contributions from seawater ( CDIC ) and an isotopically Lurifax vitreus (n ¼ 1). These also show variable preservation, lighter-DIC source. Owing to the very low concentration of but in general the shells that were originally aragonitic (the gas- inorganic carbon in serpentinization fluids, the most likely origin 13 tropods and clams) show more dissolution and recrystallization for this C depleted DIC is the oxidation of methane. Methane than the mixed calcite/aragonite mussel shells, an observation in serpentinization fluids are characterized by light carbon isoto- consistent with prolonged seawater interaction (Fig. S5). The δ13 ¼ −7‰ pic signatures (e.g., CCH4 in the Zambales ophiolite, Ghost City mollusk assemblage shares five taxa with living MAR −10 3‰ −16 7‰ −11 9‰ . at Logatchev, . at Rainbow, and . at axial high-temperature vent communities (3, 52–54), including – Lost City) (42 45), which can be further fractionated by metha- two locally at Rainbow (Bathymodiolus and Protolira), and two notrophic microbes converting methane into inorganic carbon. taxa associated with sedimented vent sites (Table S3). The Ghost While abiotic methane oxidation is kinetically inhibited at low City Phreagena sp. is also found at the recently described Clam- temperature (46), microbial oxidation of methane can occur in stone site, an inactive (approximately 25 kry BP) serpentine- subseafloor habitats with various electron acceptors (e.g., oxygen hosted sedimented vent field near Rainbow (approximately and sulfate) during the mixing of seawater with end-member 1.2 km east of Ghost City, at a depth of 1,980 m) (55). Thyasirid fluids (47, 48). According to Proskurowski et al. (48), the fractio- clams that may be conspecific with the Ghost City Thyasira sp. nation factor resulting of anaerobic or aerobic methane oxidation occur at Clamstone (55), Anya’s Garden, a sedimented vent site can be as high as 1.039 (49, 50) and will result in further depletion in the Logatchev area (52, 56, 57), and have also been reported in of the initial carbon isotopic ratio by at least −13‰. Only a small fraction (approximately 5%) of this 13C depleted methane is thus sufficient to explain the slightly negative carbon isotopic signa- ture of some Ghost City carbonates. An additional contribution from biogenic methane formed during the subseafloor mixing of seawater and the end-member fluid, as described in Proskurowski et al. (48), cannot be ruled out. This assumption is supported by the identification of both methanogenic and anaerobic methane- oxidizing at Lost City, particularly in the less active chimneys where seawater mixing is occurring (28). In Lost City- − type conditions, seawater is the only source of HCO3 , and mixing is required to compensate the poor supply of this from the fluid. As a consequence, the substantial isotopic fractionation resulting of biogenic methane formation that was observed at -hosted diffuse vents (48) may not be achieved due to limit- ing inorganic carbon conditions. The relative importance of biogenic methane is therefore difficult to estimate from Ghost City samples’ isotopic ratios. The geological context, as well as petrographic and isotopic data, provides supporting evidence that the Ghost City carbo- nates were formed 110,000 years ago from venting of metal-poor fluids. Despite the proximity with the Rainbow high-temperature vents field, the lack of polymetallic sulfide precipitates in the Ghost City carbonate samples precludes a high-temperature me- tal-rich hydrothermal fluid contribution in their formation. More GEOLOGY likely, these fluids were formed from low-temperature hydrother- mal circulation related to serpentinization and were probably close in composition to those currently venting at Lost City. Ghost City Fossils We counted 146 specimens of the mussel Bathymodiolus aff. azor- icus on the exposed surfaces of the eight Ghost City carbonate blocks (Fig. 4 and Fig. S4). The shells range in length from 5 mm to 84 mm, which is comparable to living B. azoricus shells Fig. 4. Fossils from Ghost City carbonates. (A) Carbonate block with numer- from high-temperature hydrothermal vent fields on the MAR ous specimens of Bathymodiolus aff. azoricus, showing varying degrees of (51). Very few of the Ghost City mussel shells are fragmented, shell preservation. (B) Silicone rubber cast of vesicomyid bivalve Phreagena, and quite a few specimens have articulated valves, with a ratio right valve interior. (C) Thyasirid bivalve, left valve interior. (D) Gastropod Lur- of 3.6 disarticulated to articulated shells (n ¼ 73). Some of the ifax vitreus, oblique apertural view. (E) Gastropod Anatoma sp., oblique view of damaged specimen. (F) Silicone rubber cast of gastropod Phymorhynchus small articulated mussel shells are nested within larger articulated sp., side view. (G) Silicone rubber cast from carbonate containing three specimens (Fig. 2D). These features are indicative of in situ Protolira aff. thorvaldssoni gastropod specimens (black arrows) and a single growth and a lack of post mortem transport. This interpretation limpet (white arrow). (H) Limpet Paralepetopsis aff. ferrugivora, abapertural is supported by the isotope composition of the Ghost City B. aff. view of slightly corroded specimen.

Lartaud et al. PNAS ∣ May 10, 2011 ∣ vol. 108 ∣ no. 19 ∣ 7701 Downloaded by guest on September 29, 2021 soft sediments at Lost City (20). Thus, the Ghost City mollusk to date. Our results indicate that exposed mantle rocks under- fauna is a mixture of MAR vent species from sedimented sites going serpentinization could host deep-sea chemosynthetic vent and more typical chimney habitat mussel bed communities. communities in a wide range of geological settings, including slow Although Ghost City fauna has a higher biomass, the mollusc and ultraslow spreading ridge axes, off-axis Oceanic Core Com- species list is not greatly different from Lost City communities, plexes (61), continental margins (62), and serpentinite seamounts with three mollusk species shared between the two sites: B. azor- in forearc settings (63). The exploration of expo- icus, Thyasira species, and the gastropod Lurifax (see Table S3). sures in the deep sea is thus a fertile area for the understanding both long-range larval dispersal of vent species and the specific High-Biomass Vent Communities Supported by requirements for settlement and growth of chemosynthetic Serpentinization Fluids animals. The Ghost City carbonates demonstrate that (i) high-biomass populations of Bathymodiolus mussels and other symbiont- Methods hosting mollusks can be supported by metal-depleted and likely XRD Analyses. Analyses of carbonate matrix, oxide crust, and mussel shells alkaline fluids, similar to the serpentinization-related vent fluids were made at the ISTeP laboratory (UPMC Univ Paris 06) on a Siemens described at Lost City; and (ii) these communities have been D501. Bathymodiolus aff. azoricus mussel shells were scrubbed in distilled present on the axis of the MAR for at least 110,000 years. The water with a toothbrush immediately upon collection to remove loosely flexible B. azoricus dual symbiosis responds to variations in the attached biogenic and inorganic particles. Sample powders of original calcitic methane-to-sulfide ratio in the environment (24, 25), making this outer layer and aragonitic inner layer of the shells were drilled from a depth of approximately 0.1 mm. species particularly well adapted to the variety of fluid chemis- tries that are found on the MAR (8, 58). The Ghost City fossil Optical Petrography. Polished thin sections of carbonates were observed mussels might therefore also have relied on methanotrophy and, using a stereomicroscope Zeiss SteREO Discovery V20 (Fig. 2 and Fig. S1) potentially, on sulfide, or even hydrogen, oxidation as primary Porosity measurements were made using JMicrovision software (www. energy pathways. Although the geological setting is different, jmicrovision.com). there is evidence that some other Bathymodiolus species are able to exploit diverse energy sources present in a serpentinization Carbon and Oxygen Stable Isotopes Analyses. Analyses of three Bathymodiolus context. At the South Chamorro serpentinite seamount in the aff. azoricus shells and 13 carbonate matrix (authigenic carbonate and infill- Mariana forearc, mussels thrive in sedimented cracks in seafloor ing pelagic sediments) Ghost City samples were made on a VG Micromass 602 carbonate cement, and based on soft tissue carbon and sulfur mass spectrometer. Additionally, five shells of living B. azoricus from the Rain- isotopic data, Yamanaka et al. (41) suggest that the mussels host bow vent field were analyzed. Powdered samples from mussel shells for the isotopic analyses (3–4 mg) were obtained from the cleaned outer layer using both methanotrophic and thiotrophic symbionts, utilizing both a rotary drill with a diamond-tipped burr. The shell sample powders were methane from serpentinization reactions and sulfur produced pretreated with 1.5 % NaClO for 30 min to remove organic contaminants, by sulfate reducing bacteria in the sediment. Additionally, vesi- rinsed three times with distilled water following a protocol modified after comyids (4, 59) and many of the studied large thyasirid (4, 52) (64, 65). All carbonate powders were acidified in 100% phosphoric acid at species host sulfide-oxidizing symbionts, and the presence of 50 °C under vacuum. The produced CO2 was collected and analyzed using representative species in the Ghost City carbonates suggests that the mass spectrometer. Isotopic data are reported in conventional delta a threshold amount of sulfide was present in the Ghost City (δ) notation relative to the Vienna Pee Dee Belemnite (VPDB). The standard environment. used for the analyses was an internal standard calibrated on the NBS-19. Standard deviation for δ18Oandδ13Cis0.10‰. Implications It is unclear why communities of symbiont-hosting molluscs, Uranium/Thorium and Strontium Analyses. Analyses were made in the Pôle including high densities of large Bathymodiolus mussels, do not Spectrométrie Océan (Brest) on a Neptune MC-ICPMS. For uranium and thor- ium isotope measurements, about 2 mg of carbonate sample was dissolved currently persist at Lost City, when they have been present in 236 229 in 7.5M HNO3 and spiked with a mixed U∕ Th spike (66). U and Th the past as shown by accumulations of dead shells. Because Bath- were separated chemically using conventional anion exchange techniques ymodiolus azoricus is able to exploit variable chemical energy adapted from previous studies (67). U and Th concentrations and isotope sources, the most likely explanation is to be searched for in the ratios were then measured in the MC-ICPMS. The carbonate age was cor- ecological processes that govern community dynamics in frag- rected for detrital contamination (inherited 230Th) using measured 232Th mented habitats. One possible cause of this extinction may be concentrations and assuming a typical 232Th∕230Th ratio (150,000) for the con- related to the dispersal potential of vent species. Lost City is taminant detrital phase, but this correction was insignificant on the calcu- located further from the ridge axis than Ghost City and may lated age (about 1%) (68). Strontium was isolated using Sr resin and the isotope ratios were measured using the MC-ICPMS. Isotope ratios were have lacked of sufficient larval flow from high-temperature Rain- 86 ∕88 ¼ 0 1194 87 86 bow-like vent field communities after a major disturbance event. normalized to Sr Sr . and corrected from Rb and Kr interfer- ences on the 87Sr and 86Sr signal, respectively. Another explanation could be that the focused flow chimney complex at Lost City lacks the mild temperature diffuse flow 15 ACKNOWLEDGMENTS. We thank captain and crew of R/V L’Atalante; the areas (< °C) with substantial concentrations of electron donors remotely operated vehicle Victor operation group; the MoMARDREAM scien- like methane or sulfide, that characterize suitable habitat for vent tific party for their support during the MoMARDREAM cruise; E. Rongemaille, mussels (22). Further investigation of Lost City habitat conditions N.-C. Chu, and E. Ponzevera for analytical work; E. Krylova for vesicomyid and and population genetics will help discriminating between these thyasirid bivalve identification; and A. Wáren for benthic gastropod identi- fication. T.M. Shank and A.L. Meistertzheim are also thanked for their helpful hypotheses. comments. The manuscript also benefited from helpful comments from The findings further support the hypothesis of a widespread G. Proskurowski and one anonymous reviewer. Centre National de la occurrence of hydrothermal fluid circulation hosted in exposed Recherche Scientifique (CNRS)-INSU, CNRS-INEE, IFREMER, and GENAVIR ultramafic rocks on the ocean floor (60). The estimated duration are gratefully acknowledged for their financial and technical support. The study was part of the CHEMECO collaborative project from the ESF of serpentinization-related fluid venting (over 10 kyr to 100 kyr EUROCORES EURODEEP and benefited from the joint support of Fondation time scales) (32) contrasts strongly with the geographically TOTAL and UPMC to the chair “Extreme environment, biodiversity and global restricted and short-lived high-temperature vent fields known change.”

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